The pentatricopeptide repeat protein OTP82 is required for RNA editing of plastid ndhB and ndhG transcripts

Plant Journal

Volumn 61, Issue 2, 2010, Pages 339-349

  Okuda, Kenji ^a   Hammani, Kamel ^b   Tanz, Sandra K ^b   Peng, Lianwei ^a   Fukao, Yoichiro ^c   Myouga, Fumiyoshi ^d   Motohashi, Reiko ^e   Shinozaki, Kazuo ^d   Small, Ian ^b   Shikanai, Toshiharu ^a  

^a KYOTO UNIVERSITY   (Japan)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^c NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

^d RIKEN Center for Sustainable Resource Science   (Japan)

^e SHIZUOKA UNIVERSITY   (Japan)

Author keywords

Arabidopsis; DYW motif; NAD(P)H dehydrogenase; Pentatricopeptide repeat (PPR) protein; Plastid; RNA editing

Indexed keywords

ARABIDOPSIS PROTEIN; CHLOROPLAST RNA; GREEN FLUORESCENT PROTEIN; NDHB PROTEIN, ARABIDOPSIS; NDHG PROTEIN, ARABIDOPSIS; PENTATRICOPEPTIDE REPEAT PROTEIN, ARABIDOPSIS; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE;

AMINO ACID SEQUENCE; ARTICLE; CHLOROPLAST; GENETICS; IMMUNOBLOTTING; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEIC ACID HYBRIDIZATION; NUCLEOTIDE SEQUENCE; PHOTOSYSTEM I; PROTEIN BINDING; RNA EDITING; SEQUENCE HOMOLOGY; TRANSGENIC PLANT;

AMINO ACID SEQUENCE; ARABIDOPSIS PROTEINS; BASE SEQUENCE; CHLOROPLASTS; GREEN FLUORESCENT PROTEINS; IMMUNOBLOTTING; MOLECULAR SEQUENCE DATA; MUTATION; NADH DEHYDROGENASE; NUCLEIC ACID HYBRIDIZATION; PHOTOSYSTEM I PROTEIN COMPLEX; PLANTS, GENETICALLY MODIFIED; PROTEIN BINDING; RNA EDITING; RNA, CHLOROPLAST; SEQUENCE HOMOLOGY, AMINO ACID;

ARABIDOPSIS;

EID: 73849142685     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2009.04059.x     Document Type: Article

References (51)

1. Barkan, A. Goldschmidt-Clermont, M. (2000) Participation of nuclear genes in chloroplast gene expression. Biochimie, 82, 559 572.
2. Barkan, A., Klipcan, L., Ostersetzer, O., Kawamura, T., Asakura, Y. Watkins, K.P. (2007) The CRM domain: an RNA binding module derived from an ancient ribosome-associated protein. RNA, 13, 55 64.
3. Bentolila, S., Elliott, L.E. Hanson, M.R. (2008) Genetic architecture of mitochondrial editing in Arabidopsis thaliana. Genetics, 178, 1693 1708.
4. Bock, R., Hermann, M. Fuchs, M. (1997) Identification of critical nucleotide positions for plastid RNA editing site recognition. RNA, 3, 1194 1200.
5. Cai, W., Ji, D., Peng, L., Guo, J., Ma, J., Zou, M., Lu, C. Zhang, L. (2009) LPA66 is required for editing psbF chloroplast transcripts in Arabidopsis. Plant Physiol. 150, 1260 1271.
6. Carrie, C., Murcha, M.W., Millar, A.H., Smith, S.M. Whelan, J. (2007) Nine 3-ketoacyl-CoA thiolases (KATs) and acetoacetyl-CoA thiolases (ACATs) encoded by five genes in Arabidopsis thaliana are targeted either to peroxisomes or cytosol but not mitochondria. Plant Mol. Biol. 63, 97 108.
7. Carrie, C., Kühn, K., Murcha, M.W., Duncan, O., Small, I.D., O'Toole, N. Whelan, J. (2009) Approaches to defining dual-targeted proteins in Arabidopsis. Plant J. 57, 1128 1139.
8. Chateigner-Boutin, A.L. Small, I. (2007) A rapid high-throughput method for the detection and quantification of RNA editing based on high-resolution melting of amplicons. Nucleic Acids Res. 35, e114.
9. Chateigner-Boutin, A.L., Ramos-Vega, M., Guevara-Garcia, A. et al. (2008) CLB19, a pentatricopeptide repeat protein required for editing of rpoA and clpP chloroplast transcripts. Plant J. 56, 590 602.
10. Chaudhuri, S. Maliga, P. (1996) Sequences directing C to U editing of the plastid psbL mRNA are located within a 22 nucleotide segment spanning the editing site. EMBO J. 15, 5958 5964.
11. Delannoy, E., Stanley, W.A., Bond, C.S. Small, I.D. (2007) Pentatricopeptide repeat (PPR) proteins as sequence-specificity factors in post-transcriptional processes in organelles. Biochem. Soc. Trans. 35, 1643 1647.
12. Emanuelsson, O., Nielsen, H., Brunak, S. von Heijne, G. (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J. Mol. Biol. 300, 1005 1016.
13. Giege, P. Brennicke, A. (1999) RNA editing in Arabidopsis mitochondria effects 441 C to U changes in ORFs. Proc. Natl Acad. Sci. USA, 96, 15324 15329.
14. Hashimoto, M., Endo, T., Peltier, G., Tasaka, M. Shikanai, T. (2003) A nucleus-encoded factor, CRR2, is essential for the expression of chloroplast ndhB in Arabidopsis. Plant J. 36, 541 549.
15. Hirose, T. Sugiura, M. (2001) Involvement of site-specific trans-acting factor and a common RNA-binding protein in the editing of chloroplast mRNAs: development of a chloroplast in vitro RNA editing system. EMBO J. 20, 1144 1152.
16. Inada, M., Sasaki, T., Yukawa, M., Tsudzuki, T. Sugiura, M. (2004) A systematic search for RNA editing sites in pea chloroplasts: an editing event causes diversification from the evolutionarily conserved amino acid sequence. Plant Cell Physiol. 45, 1615 1622.
17. Ito, T., Motohashi, R., Kuromori, T., Noutoshi, Y., Seki, M., Kamiya, A., Mizukado, S., Sakurai, T. Shinozaki, K. (2005) A resource of 5,814 dissociation transposon-tagged and sequence-indexed lines of Arabidopsis transposed from start loci on chromosome 5. Plant Cell Physiol. 46, 1149 1153.
18. Kim, S.R., Yang, J.I., Moon, S., Ryu, C.H., An, K., Kim, K.M., Yim, J. An, G. (2009) Rice OGR1 encodes a pentatricopeptide repeat-DYW protein and is essential for RNA editing in mitochondria. Plant J. 59, 738 749.
19. Kobayashi, Y., Matsuo, M., Sakamoto, A., Wakasugi, T., Yamada, K. Obokata, J. (2007) Two RNA editing sites with cis-elements of moderate sequence identity are recognized by an identical site-recognition protein in tobacco chloroplasts. Nucleic Acids Res. 36, 311 318.
20. Kotera, E., Tasaka, M. Shikanai, T. (2005) A pentatricopeptide repeat protein is essential for RNA editing in chloroplasts. Nature, 433, 326 330.
21. Kroeger, T.S., Watkins, K.P., Friso, G., van Wijk, K.J. Barkan, A. (2009) A plant-specific RNA binding domain revealed through analysis of chloroplast group II intron splicing. Proc. Natl Acad. Sci. USA, 106, 4537 4542.
22. Kuromori, T., Hirayama, T., Kiyosue, Y., Takabe, H., Mizukado, S., Sakurai, T., Akiyama, K., Kamiya, A., Ito, T. Shinozaki, K. (2004) A collection of 11,800 single-copy Ds transposon insertion lines in Arabidopsis. Plant J. 37, 897 905.
23. Lurin, C., Andres, C., Aubourg, S. et al. (2004) Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell, 16, 2089 2103.
24. Lutz, K.A. Maliga, P. (2001) Lack of conservation of editing sites in mRNAs that encode subunits of the NAD(P)H dehydrogenase complex in plastids and mitochondria of Arabidopsis thaliana. Curr. Genet. 40, 214 219.
25. Munekage, Y., Hashimoto, M., Miyake, C., Tomizawa, K., Endo, T., Tasaka, M. Shikanai, T. (2004) Cyclic electron flow around photosystem I is essential for photosynthesis. Nature, 429, 579 582.
26. Murcha, M.W., Elhafez, D., Lister, R., Tonti-Filippini, J., Baumgartner, M., Philippar, K., Carrie, C., Mokranjac, D., Soll, J. Whelan, J. (2007) Characterization of the preprotein and amino acid transporter gene family in Arabidopsis. Plant Physiol. 143, 199 212.
27. Nakamura, T. Sugita, M. (2008) A conserved DYW domain of the pentatricopeptide repeat protein possesses a novel endoribonuclease activity. FEBS Lett. 582, 4163 4168.
28. O'Toole, N., Hattori, M., Andres, C., Iida, K., Lurin, C., Schmitz-Linneweber, C., Sugita, M. Small, I. (2008) On the expansion of the pentatricopeptide repeat gene family in plants. Mol. Biol. Evol. 25, 1120 1128.
29. Okuda, K., Nakamura, T., Sugita, M., Shimizu, T. Shikanai, T. (2006) A pentatricopeptide repeat protein is a site recognition factor in chloroplast RNA editing. J. Biol. Chem. 281, 37661 37667.
30. Okuda, K., Myouga, F., Motohashi, R., Shinozaki, K. Shikanai, T. (2007) Conserved domain structure of pentatricopeptide repeat proteins involved in chloroplast RNA editing. Proc. Natl Acad. Sci. USA, 104, 8178 8183.
31. Okuda, K., Habata, Y., Kobayashi, Y. Shikanai, T. (2008) Amino acid sequence variations in Nicotiana CRR4 orthologs determine the species-specific efficiency of RNA editing in plastids. Nucleic Acids Res. 36, 6155 6164.
32. Okuda, K., Chateigner-Boutin, A., Nakamura, T., Delannoy, E., Sugita, M., Myouga, F., Motohashi, R., Shinozaki, K., Small, I. Shikanai, T. (2009) Pentatricopeptide repeat proteins with the DYW motif have distinct molecular functions in RNA editing and RNA cleavage in Arabidopsis chloroplasts. Plant Cell, 21, 146 156.
33. Peng, L., Ma, J., Chl, W., Guo, J., Zhu, S., Lu, Q., Lu, C. Zhang, L. (2006) Low PSII accumulation1 is involved in efficient assembly of photosystem II in Arabidopsis thaliana. Plant Cell, 18, 955 969.
34. Peng, L., Shimizu, H. Shikanai, T. (2008) The chloroplast NAD(P)H dehydrogenase complex interacts with photosystem I in Arabidopsis. J. Biol. Chem. 83, 34873 34879.
35. Peng, L., Fukao, Y., Fujiwara, M., Takami, T. Shikanai, T. (2009) Efficient operation of NAD(P)H dehydrogenase requires the supercomplex formation with photosystem I via minor LHCI in Arabidopsis. Plant Cell, doi :.
36. Robbins, J.C., Heller, W.P. Hanson, M.R. (2009) A comparative genomics approach identifies a PPR-DYW protein that is essential for C-to-U editing of Arabidopsis chloroplast accD transcript. RNA, 15, 1142 1153.
37. Rüdinger, M., Polsakiewicz, M. Knoop, V. (2008) Organellar RNA editing and plant-specific extensions of pentatricopeptide repeat proteins in jungermanniid but not in marchantiid liverworts. Mol. Biol. Evol. 25, 1405 1414.
38. Salone, V., Rüdinger, M., Polsakiewicz, M., Hoffmann, B., Groth-Malonek, M., Szurek, B., Small, I., Knoop, V. Lurin, C. (2007) A hypothesis on the identification of the editing enzyme in plant organelles. FEBS Lett. 581, 4132 4138.
39. Sasaki, T., Yukawa, Y., Miyamoto, T., Obokata, J. Sugiura, M. (2003) Identification of RNA editing siets in chloroplast transcripts from the maternal and paternal progenitors of tobacco (Nicotiana tabacum): comparative analysis shows the involvement of distinct trans-factors for ndhB editing. Mol. Biol. Evol. 20, 1028 1035.
40. Schmitz-Linneweber, C. Small, I. (2008) Pentatricopeptide repeat proteins: a socket set for organelle gene expression. Trends Plant Sci. 13, 663 670.
41. Shikanai, T. (2006) RNA editing in plant organelles: machinery, physiological function and evolution. Cell. Mol. Life Sci. 63, 698 708.
42. Shikanai, T., Endo, T., Hashimoto, T., Yamada, Y., Asada, K. Yokota, A. (1998) Directed disruption of the tobacco ndhB gene impairs cyclic electron flow around photosystem I. Proc. Natl Acad. Sci. USA, 95, 9705 9709.
43. Small, I.D. Peeters, N. (2000) The PPR motif - a TPR-related motif prevalent in plant organellar proteins. Trends Biochem. Sci. 25, 46 47.
44. Small, I., Peeters, N., Legeai, F. Lurin, C. (2004) Predotar: a tool for rapidly screening proteomes for N-terminal targeting sequences. Proteomics, 4, 1581 1590.
45. Takenaka, M., Neuwirt, J. Brennicke, A. (2004) Complex cis-elements determine an RNA editing site in pea mitchoncdria. Nucleic Acids Res. 32, 4137 4144.
46. Timmis, J.N., Ayliffe, M.A., Huang, C.Y. Martin, W. (2004) Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat. Rev. Genet. 5, 123 135.
47. Tsudzuki, T., Wakasugi, T. Sugiura, M. (2001) Comparative analysis of RNA editing sites in higher plant chloroplasts. J. Mol. Evol. 53, 327 332.
48. Yu, Q.B., Jiang, Y., Chong, K. Yang, Z.N. (2009) AtECB2, a pentatricopeptide repeat protein, is required for chloroplast transcript accD RNA editing and early chloroplast biogenesis in Arabidopsis thaliana. Plant J. 59, 1011 1023.
49. Zehrmann, A., van der Merwe, J.A., Verbitskiy, D., Brennicke, A. Takenaka, M. (2008) Seven large variations in the extent of RNA editing in plant mitochondria between three ecotypes of Arabidopsis thaliana. Mitochondrion, 8, 319 327.
50. Zehrmann, A., Verbitsky, D., van der Merwe, J.A., Brennicke, A. Takenaka, M. (2009) A DYW domain-containing pentatricopeptide repeat proteins is required for RNA editing at multiple sites in mitochondria of Arabidopsis thaliana. Plant Cell, 21, 558 567.
51. Zhou, W., Cheng, Y., Yap, A., Chateigner-Boutin, A.L., Delannoy, E., Hammani, K., Small, I. Huang, J. (2008) The Arabidopsis gene YS1 encoding a DYW protein is required for editing of rpoB transcripts and the rapid development of chloroplasts during growth. Plant J. 58, 82 96.